Phytophthora: an ancient, historic, biologically and structurally cohesive and evolutionarily successful generic concept in need of preservation

The considerable economic and social impact of the oomycete genus Phytophthora is well known. In response to evidence that all downy mildews (DMs) reside phylogenetically within Phytophthora, rendering Phytophthora paraphyletic, a proposal has been made to split the genus into multiple new genera. We have reviewed the status of the genus and its relationship to the DMs. Despite a substantial increase in the number of described species and improvements in molecular phylogeny the Phytophthora clade structure has remained stable since first demonstrated in 2000. Currently some 200 species are distributed across twelve major clades in a relatively tight monophyletic cluster. In our assessment of 196 species for twenty morphological and behavioural criteria the clades show good biological cohesion. Saprotrophy, necrotrophy and hemi-biotrophy of woody and non-woody roots, stems and foliage occurs across the clades. Phylogenetically less related clades often show strong phenotypic and behavioural similarities and no one clade or group of clades shows the synapomorphies that might justify a unique generic status. We propose the clades arose from the migration and worldwide radiation ~ 140 Mya (million years ago) of an ancestral Gondwanan Phytophthora population, resulting in geographic isolation and clade divergence through drift on the diverging continents combined with adaptation to local hosts, climatic zones and habitats. The extraordinary flexibility of the genus may account for its global ‘success’. The 20 genera of the obligately biotrophic, angiosperm-foliage specialised DMs evolved from Phytophthora at least twice via convergent evolution, making the DMs as a group polyphyletic and Phytophthora paraphyletic in cladistic terms. The long phylogenetic branches of the DMs indicate this occurred rather rapidly, via paraphyletic evolutionary ‘jumps’. Such paraphyly is common in successful organisms. The proposal to divide Phytophthora appears more a device to address the issue of the convergent evolution of the DMs than the structure of Phytophthora per se. We consider it non-Darwinian, putting the emphasis on the emergent groups (the DMs) rather than the progenitor (Phytophthora) and ignoring the evolutionary processes that gave rise to the divergence. Further, the generic concept currently applied to the DMs is narrower than that between some closely related Phytophthora species. Considering the biological and structural cohesion of Phytophthora, its historic and social impacts and its importance in scientific communication and biosecurity protocol, we recommend that the current broad generic concept is retained by the scientific community. Supplementary Information The online version contains supplementary material available at 10.1186/s43008-022-00097-z.


INTRODUCTION
The era of molecular phylogeny has provided strong evidence that the downy mildews (DMs) are as a group polyphyletic, having evolved at least twice from Phytophthora ancestors (Cooke et al. 2000;Runge et al. 2011;Jung et al. 2017a;Bourret et al. 2018;Scanu et al. 2021). This has led to a proposal to distribute the main phylogenetic clades of Phytophthora among several new genera (Runge et al. 2011), further indicated recently by Crous et al. (2021a). To assess the merits of this proposal we review here the environmental, economic and social impact, and the biological and phylogenetic characteristics of the genus, including its relationship to the DMs. We conclude that the case for retaining Phytophthora as a single genus is overwhelming.

Historical background
Phytophthora is arguably the world's most historic and economically significant genus in plant pathology. A comprehensive timeline of milestones for the genus is given in Table 1. In current classifications Phytophthora is usually assigned to the phylum Oomycota, which in turn are widely accepted as belonging to the heterokont algal-derived, but still somewhat debated, Straminipila within the kingdom Chromista (Dick 2001;Beakes et al. 2012). Together with other oomycetes, Phytophthoras are diploid with gametangial meiosis (Sansome 1961(Sansome , 1965) and a genetic system akin to that of vascular plants (Brasier 1992;Goodwin 1997). They form indeterminate sporangiophores bearing alga-like sporangia that, in turn, release flagellate zoospores; and alga-like sexual oogonia and antheridia. Like most oomycetes, Phytophthoras exhibit a strong dependence on free water or high humidity for sporangial formation, zoospore spread and infection.
Within the oomycetes, Phytophthora is now assigned to the order Peronosporales, the vast majority of which are plant pathogens (Runge et al. 2011;Thines and Choi 2016;Jung et al. 2017aJung et al. , 2018a. Amongst others this order includes the genera Halophytophthora and Calycofera, Phytophthora's sister genus Nothophytophthora, and 20 genera of DMs including Bremia, Peronospora, Plasmopara and Sclerospora (cf. Thines and Choi 2016;Jung et al. 2017a;McCarthy and Fitzpatrick 2017;Bourret et al. 2018;Scanu et al. 2021;Maia et al. 2022). Phytophthora and Nothophytophthora are mainly soil and water inhabiting, necrotrophic to hemibiotrophic pathogens forming zoosporic sporangia, whereas the DMs are aerial, obligate biotrophic pathogens with often conidia-like sporangia. The first DM genus, Peronospora, was erected by Corda (1837). The nomenclatural history of Phytophthora began with the potato blight epidemic in western Europe in the 1840s that led to the infamous Irish potato famine (Large 1940;Bourke 1991). The causal agent was initially named Botrytis infestans by Montagne (1845). It was then redesignated Peronospora trifurcata by Unger (1847), Peronospora infestans by Caspary in (1853) (published in Rabenhorst's Herbarium vivum Mycologicum exsiccati no. 1879), and finally renamed Phytophthora infestans by de Bary (1876), with P. infestans as the 'type species' for the new genus Phytophthora (Table 1).

Rapid increase in described Phytophthora species
From around 2000 the number of described species increased rapidly. This was partly due to the unravelling of morphospecies complexes by combinations of classical and molecular methods (e.g. Brasier et al. 2003;Hansen et al. 2019;Jung et al. 2011;Bertier et al. 2013;Ginetti et al. 2014;Safaiefarhani et al. 2015;Weir et al. 2015); and partly to the discovery of many new species and infraspecific lineages during dedicated surveys in forests and natural ecosystems, especially remote regions with low accessibility (e.g. Jung et al. 2003Jung et al. , 2011Jung et al. , 2017bJung et al. , c, d, 2018bJung et al. , 2020Jung et al. , 2021Rea et al. 2011;Reeser et al. 2011;Brasier et al. 2012;Scanu et al. 2015;Burgess et al. 2018;Dang et al. 2021). Within a decade the number of formally described Phytophthoras had surpassed 100, and it was estimated that the number of extant Phytophthora species could be between 200 and 600 (Brasier 2009). Currently, the number of formally described and accepted taxa has reached 200 Chen et al. 2022) and many other new taxa have been designated informally (Brasier et al. 2003;Hüberli et al. 2013;Oh et al. 2013;Jung et al. 2017dJung et al. , 2018bJung et al. , 2020. Another 2-400 species may remain to be discovered in the world's unsurveyed forests and natural ecosystems (Brasier 2009). Figure 1 summarises the numerical chronology of described Phytophthora species, highlighting the exponential increase in species numbers over the past two decades.

Economic, environmental and social impact of the genus
Having been born out of a disastrous famine in Western Europe the genus Phytophthora was imbued with a degree of notoriety from its inception. Any modern perception of the genus needs to be much broader, in part because a definition of 'importance' in solely human terms is an artificial, not a biological, construct: P. infestans is no more biologically significant in its natural environment than are most other Phytophthoras in theirs. Nonetheless the genus contains a remarkable number of individually infamous pathogens, including (in addition to P. infestans) P. capsici, P. cinnamomi, P. megakarya, P. nicotianae, P. palmivora, P. plurivora and P. ramorum. Overall, the anthropogenically-related impacts of Phytophthoras are enormous (Tables 2, 3, Additional files 1, 2: Tables S1, S2). Most of these impacts are driven by introductions to environments with highly susceptible hosts, use of crop monocultures, host stress due to 'offsite' cultivation and climate change, or a combination of these (e.g. Brasier and Scott 1994;Erwin and Ribeiro 1996;Jung 2009;Jung et al. 2000Jung et al. , 2018aRizzo et al. 2002; Fig. 1 Number of described and accepted Phytophthora species over time. Adapted from Brasier (2009). Data from pre-molecular era publications (Tucker 1931;Waterhouse 1970;Stamps et al. 1990;Erwin and Ribeiro 1996) include only those species currently accepted as valid species Page 5 of 25 Brasier et al. IMA Fungus (2022) 13:12 Table 3 Examples of the ecological, economic and social impacts of disease syndromes or processes involving multiple Phytophthora species a Lists of the individual taxa involved in each syndrome (including described species and currently informally designated species) and the full citations of the associated references are shown in Additional file 2: where significant damage is done to human communities with outcomes ranging from starvation, death and mass migration to loss of cultural heritage (Tables 2, 3, Additional files 1, 2: Tables S1, S2). In some cases, the impact factors are multiple. For example, the introduced P. cinnamomi causes damage to native forests and to important Mediterranean heath ecosystems and is also a serious problem in commercial nurseries and in horticultural and forest plantations (Brasier et al. 1993;Erwin and Ribeiro 1996;Shearer et al. 2004;Jung et al. 2016Jung et al. , 2018aJung et al. , 2020. In Australia P. cinnamomi is considered a key threatening process to the Australian estate under the Environment Protection and Biodiversity Conservation Act 1999. The introduction of P. ramorum has had a considerable impact on the ornamental nursery trade in North America and Europe, caused heavy losses of native tanoaks (Neolithocarpus densiflorus) in the USA and commercial larch (Larix kaempferi) plantations in the UK, and collateral damage to many adjacent tree and shrub species and native ericaceous heaths (e.g. Rizzo et al. 2002;Brasier and Webber 2010;Jung et al. 2016Jung et al. , 2018a. The loss of oak and tanoak acorns has affected native American culture (e.g. Ortiz 2008) and food sources for wildlife. Many disease syndromes or processes involve multiple Phytophthora species (Tables 3, Additional file 2: Table S2). Since the 1990s, the number Page 10 of 25 Brasier et al. IMA Fungus (2022) 13:12 of previously unknown Phytophthora declines of forests and natural ecosystems globally has increased exponentially, from 11 to currently 41 (Fig. 2). The number of publications and citations for selected Phytophthoras is also indicated in Table 2. Again, this should not be automatically interpreted as indicating the 'relative importance' of a species. While they do to an extent reflect a species' scientific profile, such statistics can also be biased by the length of time a problem has been recognised; the economic value of particular cash crops-especially food crops; exacerbation of problems by subsequent disease management or biosecurity breaches; and the often more generous research grants available in developed countries. Furthermore, publications and citations related to environmental impacts, even major impacts such as loss of Kauri pines (Agathis robusta) to P. agathidicida in New Zealand, or loss of entire species-rich heath vegetation in southwest Australia to P. cinnamomi (Table 2, Additional file 3:  Table S3), tend to be substantially fewer, usually as a consequence of limited research funding.

The monophyly of Phytophthora and the sustained structural stability of its phylogenetic clades
The first molecular phylogenetic analysis of Phytophthora and other oomycetes was published by Cooke et al. (2000). It was based on ITS profiles and included 50 described Phytophthora species. Unlike other oomycete genera such as Pythium or Halophytophthora, Phytophthora was revealed as a tight monophyletic cluster of eight major clades (Clades 1-8), plus two putatively more distantly related clades (Clades 9 and 10). Unsurprisingly, the clades were also shown to transcend previous morphological groupings. Strikingly, Peronospora sparsa clustered within Phytophthora Clade 4, indicating a relatively recent evolution of Peronospora and other DMs from Phytophthora. Cooke et al. (2000) suggested Peronospora and Bremia were obligate, conidial Phytophthoras, in support of an earlier proposal by Gäumann (1952).
Since then, at least 12 other molecular phylogenetic studies of Phytophthora have been undertaken, ranging from increasingly complex multigene analyses (Martin and Tooley 2003;Kroon et al. 2004Kroon et al. , 2012Blair et al. 2008;Robideau et al. 2011;Martin et al. 2014;Rahman et al. 2015;Jung et al. 2017c;Yang et al. 2017;Bourret et al. 2018;Scanu et al. 2021;Chen et al. 2022) to a genomewide sequence-based phylogeny (Van Poucke et al. 2021). These studies have been carried out against the background of the rapidly increasing number of described Phytophthora species outlined above.
Despite these fresh analyses and the addition of many new species our perception of the infrageneric structure of Phytophthora has changed little since Cooke et al. (2000). The overall clade structure has remained stable and generally accepted. The number of major clades, i.e. those with four or more species (therefore, excluding monospecific Clades 11, 13 and 14, currently represented by P. lilii; the undescribed P. taxon mugwort; and P. cyperi, which is probably a DM; Ho et al. 2004;Bourret et al. 2018) has increased from ten to eleven (Jung et al. 2017c;Chen et al. 2022). The phylogenetic positions of some species have been clarified and multiple new subclades have been added.
Above all, the major Phytophthora clades are still confirmed to be a relatively tight, bush-like, fundamentally monophyletic, evolutionary cluster. Indeed Clades 9 and 10, considered by Cooke et al. (2000) to be more distant, are now more closely aligned with the other major clades (Jung et al. 2017c;Yang et al. 2017;Scanu et al. 2021;Van Poucke et al. 2021;Chen et al. 2022). This is in contrast to the oomycete genus Pythium which, beginning with Cooke et al. (2000), has been shown to be evolutionarily divergent and polyphyletic, and in consequence was split into several monophyletic genera (de Cock et al. 2015;Uzuhashi et al. 2010).

Phytophthora is a biologically sound and cohesive genus
The continued acceptance by the scientific community of Phytophthora as an assemblage of clades has probably also reflected a perception that this structure exhibits strong biological cohesion. Thus, the 11 major phylogenetic clades share a wide range of characters, both morphological and behavioural, that collectively characterise the genus (Figs. 4, 5; Table 4, Additional files 3, 4, 5: Tables S3, S4, S5). Also these characters often show as much variation between species within a clade as they do between clades ( For example, caducous (deciduous) sporangia are found in nine major clades and persistent sporangia in all 11 clades ( Fig. 4; Additional file 3: Table S3). Chlamydospores are produced by 59 species in ten clades; and 137 species across all eleven clades lack the ability to produce them ( Fig. 4; Additional file 3: Table S3). Eight of the clades contain both self-fertile (homothallic) species and species with an A1/A2 outcrossing (heterothallic) breeding system. Both amphigynous and paragynous antheridia are found in eight clades ( Fig. 4; Additional file 3: Table S3). Sterile species occur in five clades.
Furthermore, phylogenetically divergent clades often share strong similarities in 'lifestyle' . An aerial dispersal lifestyle occurs across eight and a soilborne lifestyle across all 11 major clades. Apparently very flexibly-adapted species exhibiting both an aerial and a soilborne lifestyle are found in seven clades ( Fig. 5; Additional file 4: Table S4). The ability to infect and seriously damage roots, bark (phloem) and even xylem (Brown and Brasier 2007;Parke et al. 2007) tissues of woody hosts as well as herbaceous tissues is something of a Phytophthora speciality among the oomycetes, and largely distinguishes the genus from the obligately biotrophic DMs. It is found in 71.9% of the species and across all the clades (Fig. 5; Additional file 4: Table S4). Species with wide, medium and narrow host ranges and species exhibiting host specificity are found in all or nearly all clades ( Fig. 5; Additional file 4: Table S4). In addition, currently at least 85 Phytophthora species (43%), representing all 11 major clades, have been shown to disperse in an aquatic environment ( Fig. 5; Additional file 4: Table S4) and to live saprotrophically, free from the host. This property also distinguishes Phytophthora from the DMs. Forty-one species in five clades, including 25 of the 27 sterile species, have a primarily aquatic lifestyle as  Table S4). A wide adaptation to climatic conditions is another feature shared across the clades: the majority contain species with either low, medium or high cardinal temperatures for growth ( Fig. 4; Additional file 5: Table S5). Indeed, phylogenetically divergent Clades 1 and 8 are remarkably similar both in terms of the proportion of species adapted to low, medium or high optimum temperatures and in their maximum temperature tolerances (Additional file 5: Table S5). Furthermore, within each of the 21 different 'lifestyle and behavioural categories' listed in Additional files 4 and 5: Tables S4 and S5 the number of clades with taxa that exhibit the attribute is consistently high: average 9.1 across the eleven major clades; range 5-11. Cooke et al. (2000) also reviewed the morphological and behavioural properties of their 50 Phytophthora taxa and proposed that Clades 1-5 comprised predominantly aerially dispersed species with papillate caducous sporangia and Clades 6-8 predominantly soil dispersed species with persistent non-papillate sporangia, consistent with an earlier proposal for two evolutionary trends in the genus (Brasier 1983). In the present analysis and that of Yang et al. (2017) this last proposal is no longer fully supported. Of the 75 species in Clades 1-5, for example, 32% are papillate caducous and aerial, another 30.7% are papillate persistent and soil inhabiting and the remaining 36.3% represent a mixture of attributes (Additional file 6: Table S6). For Clades 6-8 however the proposal does have support. Of 89 species, 80.9% are non-papillate persistent and soil inhabiting, compared to 11.2% semi-papillate persistent and soil inhabiting and 4.5% semi-papillate and partly caducous (Additional file 6: Table S6). Clades 1-5, therefore, appear more flexible in terms of their present day 'lifestyle' variability than Clades 6-8.
Across the clades unusual developmental features are exhibited by a small number of species (Table 5, Additional file 7: Table S7). Collectively, these are another indication of the behavioural adaptability of the genus. Sporangiophore constrictions are found in P. pinifolia (Clade 6) and P. constricta (Clade 9), presumably to facilitate aerial dispersal in otherwise non-papillate, soil and waterborne species. These appear to be an example of convergent evolution (Rea et al. 2011), as do the ultra-long sporangial pedicels produced by P. capsici (Clade 2) and P. hibernalis (Clade 8) (Kunimoto  Erwin & Ribeiro 1996). These pedicels may promote sporangial clustering (cf. Granke et al. 2009) and adherence to surfaces. Also unusual are the stromata formed by P. cinnamomi (Clade 7) and by P. ramorum and P. lateralis (Clade 8) (Table 5; Moralejo et al. 2006;Brasier et al. 2010;Jung et al. 2013), which may be adaptations for nutrient storage and eruption through tough leaf or periderm surfaces.

Evolution and adaptability of the Phytophthora clades
Considering the many ecological niches and environments it has occupied, phenotypically the genus Phytophthora appears to have changed remarkably little. This raises the question of the evolutionary processes that have resulted in its clades being phylogenetically divergent, yet still exhibiting strong biological and behavioural conformity coupled with high adaptability. We suggest that the clades developed as a result of the migration and worldwide radiation of an ancestral Gondwanan or pre-Gondwanan Phytophthora population on the emerging continents, beginning around 140 Mya and that the resulting geographic isolation led to a degree of clade divergence through genetic drift, and also local adaptation to the different hosts and parts of hosts, habitats and climatic zones on the diverging continents. We suggest the sustained biological similarity across the clades (Figs. 4, 5; Table 4, Additional files 3, 4, 5: Tables S3, S4, S5) is due to the Phytophthora lifestyle and genome being highly versatile in terms of (1) switching between different spore morphologies or dispersal modes ( Fig. 4; Additional file 3: Table S3); (2) a range of trophic options from saprotrophy on degraded vegetation to necrotrophy and transient biotrophy on diverse tissues of pteridophytes, gymnosperms and angiosperms (  Table S3), including an inbreeding system ('homothallism') with probably no barrier to outbreeding (cf. Whisson et al. 1994) and an outcrossing system (A1/A2 compatibility or 'heterothallism') that also enables selfing (Sansome 1980;Brasier 1992;Judelson 2009); (4) an ability to rapidly modify host-pathogen recognition processes via effector molecules (Kamoun et al. 1997;Kamoun 2006)   Page 15 of 25 Brasier et al. IMA Fungus (2022) 13:12 significant biological change; often resulting in convergent evolution between otherwise geographically isolated clades (Figs. 4, 5; Table 4).
In summary, we consider that Phytophthora is a highly flexible and highly successful biological 'model' that has survived well over aeons of time, leading to molecularly detectable divergence between its clades without a marked disjunction in their general morphology or behaviour. This great adaptability is probably a major factor in their being high risk pathogens when introduced into new environments.

Emergence of the Downy Mildews
A major development among the Phytophthora clades has been the emergence of the DMs. On one occasion this was from a common ancestor with Clades 1-5 and Clade 12, on the other from a common ancestor with Clade 1 (Bourret et al. 2018 ; Fig. 3). This has resulted in the emergence of organisms with a broadly similar range of properties, apparently via convergent evolution. Probably the most definitive characteristics of the DMs are obligate biotrophy of angiosperms, usually accompanied by intracellular haustoria; and sporangiophores of determinate growth, facilitating synchronised dispersal. Major host shifts including adaptive radiation on particular plant families such as the Poaceae and Brassicaceae, combined with high levels of host specificity on largely herbaceous plant parts, are believed to have played a major role in their emergence (Göker et al. 2007;Thines and Choi 2016;Bourret et al. 2018). Also characteristic is aerial dissemination; and, in 10 of the 20 genera, directly germinating conidiosporangia (Gäumann 1964;Hall 1996;Göker et al. 2007;Thines and Choi 2016;Fletcher et al. 2019).
Given the adaptiveness and global spread of Phytophthoras it is perhaps surprising that this process has succeeded only twice. However, these developments involved abandoning definitive Phytophthora properties. This includes: necrotrophic ability (Thines and Choi 2016;Fletcher et al. 2018), important in Phytophthora parasitism of woody tissues and resulting in DMs being more benign pathogens or even endophytes; nutrient transporters linked to saprotrophic ability, enabling Phytophthoras nutrient gain in competition with other microorganisms; loss of the ability to utilise inorganic nitrogen and sulphur (Yin et al. 2017); loss of indefinite sporangiophore development, an adaptation best suited to continuously wet or aquatic conditions; and for many DMs, loss of the mechanism of zoosporogenesis (Fletcher et al. 2018) and therefore zoospore mediated infection. Indeed, detailed comparisons of Phytophthora and DM genomes support synteny and a common origin but also  25 Brasier et al. IMA Fungus (2022) 13:12 demonstrate that DMs have lost conserved domains encoding some of these properties (Fletcher et al. 2018(Fletcher et al. , 2021. The narrower host and nutrient specificity, reduction in the effector repertoire and consistently reduced pathogenicity gene complements of the DMs (Fletcher et al. 2018) could render DM species more prone to extinction in a changing environment (Thines and Choi 2016). Equally, by completing their life cycles in the more sheltered and homogeneous milieu of living plant tissues DMs are probably less exposed to competition from other microorganisms; and due to their host specificity at less 'risk' of interspecific hybridisation, especially compared with the ecologically more flexible Phytophthoras (Brasier 2001;Van Poucke et al. 2021). The much longer average branch lengths in the DMs, largely distinguish them from the more tightly clustered 'bush-like' Phytophthora clades, and probably reflect a relatively rapid evolution towards enhanced host specialisation and biotrophy (Bourret et al. 2018;and Fig. 3): an evolutionary jump, perhaps driven by strong directional selection associated with ensuing host-pathogen 'arms races' . In consequence, many early stages in the evolution of the DMs are probably lost to extinction. Indeed, despite the thousand or so extant Phytophthora and DM taxa, examples of prominent Phytophthora-like characters among the DMs and vice versa are patchy and often somewhat equivocal. Thines (2009) discusses what may be 'intermediate taxa' or 'bridging taxa' . But such terms are, however, subjective and should probably be treated with caution because of: (1) the unknown progenitor taxa; (2) intervening extinctions and reticulations; (3) the possibility of convergent evolution; and (4) the lack of information on the genetic control of many characters, such as haustorial form or sporangiophore development.
Amongst Phytophthoras, the recently described P. podocarpi (previously P. taxon totara) on Podocarpus shoots in New Zealand shares a common ancestor with the DMCCs and their relatives (Bourret et al. 2018) but otherwise has Phytophthora characteristics (Dobbie et al. 2022). Phytophthora litchii (syn. Peronophythora litchii) in Clade 4 resembles DMs in producing determinate sympodial sporangiophores, a 'downy white mycelium' on lychee (Litchi chinensis) fruits, and smaller gene families (Chen 1961;Ho et al. 1984;Ye et al. 2016;Sun et al. 2017). Otherwise, P. litchii causes necrotic lesions, is able to grow on artificial media, and displays a typical Phytophthora-type zoospore release and gametangial morphology. The aerial and soil inhabiting P. heterospora (also Clade 4), which causes bark and root necroses on various woody host plants, produces both zoosporereleasing sporangia and directly germinating pseudoconidia ).
The possession of such unusual characters by P. litchii and P. heterospora does not, however, confirm them as proto-DMs. The 'DM-like' characteristics of P. litchii (Tables 5, Additional file 7: Table S7) could be evidence of a common ancestor shared with the DMs, but they could also reflect convergent evolution (Ye et al. 2016) or ancestral hybridisation. The determinate sporangiophores and the 'downy' mycelium could be adaptations to reduce or avoid desiccation on the exposed surface of the leathery lychee pericarp. The downy mycelium might be more refractive due to a protective cell surface hydrophobin or mucin (cf. Meijer et al. 2006). The pseudoconidia of P. heterospora, at face value a DM-like feature, may be an adaptation allowing extra reproductive versatility in alternating moister and drier diurnal or seasonal conditions . As already discussed, there are comparable unique or unusual developmental features in other Phytophthora species (Table 5, Additional file 7: Table S7).

Phytophthora-like characters among the DMs
Ten of the 20 DM genera, including Pseudoperonospora, Plasmopara and Sclerophthora produce sporangia which release zoospores (Bourret et al. 2018). Peronospora cyperi (syn. Kawakamia cyperi), was later renamed Phytophthora cyperi, probably because of the reportedly Phytophthora-like caducous sporangia and paragynous antheridia (Erwin and Ribeiro 1996). Whether P. cyperi produces zoospores is uncertain, but it should probably be accepted under the name K. cyperi based on it being a biotroph (Thines et al. 2015) and its phylogenetic status (Bourret et al. 2018;and Fig. 3).
Three monotypic graminicolous DM genera, Graminivora, Poakatesthia and Viennotia show features not found in other DMs. In particular, the indeterminate sporangiophores and P. infestans-like sporangial apophyses in V. oplismeni, and the occurrence of intracellular hyphal growth in Poakatesthia penniseti, which casts doubt on whether it is an obligate biotroph (Thines 2009). These features were suggested by Beakes and Thines (2017) to be evolutionary hangovers from Phytophthora, but some could also reflect convergent evolution.
Perhaps the best example of a DM with Phytophthoralike characters is the graminicolous genus Sclerophthora. This is widely presumed to be biotrophic (Kenneth 1981;Erwin and Ribeiro 1996;Thines and Choi 2016) and in molecular phylogenies exhibits the characteristic long branch length, or evolutionary jump, of the DMs (Thines et al. 2008;Bourret et al. 2018). Sclerophthora macrospora has Phytophthora-like sporangiophore and sporangial morphology, and a wide but highly specialised graminicolous, and therefore non-Phytophthora-like, host range (Kenneth 1981;Erwin and Ribeiro 1996;Telle and Thines Page 17 of 25 Brasier et al. IMA Fungus (2022) 13:12 2012). Tokura (1975) reported culturing S. macrospora on artificial media but was unable to obtain zoospores or to infect rice seedlings with these cultures. Tokura's observations have yet to be repeated. Any attempt to do so will hopefully include diagnosis of any resulting axenic growth with molecular markers. Among a panoply of around 800 species across 20 DM genera it is likely that some ancestral Phytophthora-like characteristics will have survived as long as they did not confer a marked selective disadvantage. On the evidence of Thines (2009), retention of Phytophthora-like characters in the DMs is associated with particular host groups. Specifically, in Sclerophthora and Viennotia in respect of the Poaceae, and in 'P. cyperi' the Cyperaceae. Perhaps these associations involved host jumps, and possibly horizontal gene transfer (cf. Brasier 1995;Bourret et al. 2018;Fletcher et al. 2021), resulting in such closed host-pathogen systems that drivers towards further adaptation were less intense.

Proposals to split Phytophthora into separate genera are biologically and phylogenetically inappropriate Evolutionary process versus taxonomic cladism
None of the authors of the many molecular phylogenies of Phytophthora published since Cooke et al. (2000) have suggested there is a case either for a merging of the clades, or for their nomenclatural designation as subgenera or sections. This apparent acceptance of the clade structure has probably also reflected a perception of their biological cohesion and of the enormous significance of the genus for scientific communication and global biosecurity (discussed later).
Nonetheless, to resolve the paraphyly of Phytophthora, reflected in the evidence that the DMs have evolved from the genus (Cooke et al. 2000;Jung et al. 2017a;Bourret et al. 2018;Scanu et al. 2021), and applying the terminology of cladism (not to be confused with cladistics), Runge et al. (2011) proposed either (1) placing all DMs and Phytophthora species in a single genus under the oldest generic name Peronospora, which would require renaming all Phytophthora species and those in 19 DM genera, resulting in a highly heterogeneous group; or (2) the description of at least six new genera within Phytophthora in order to conserve the DM genera. We consider the first of these suggestions intrinsically flawed as it would assimilate the ancient ancestral genus Phytophthora with its broad suite of morphological and behavioural characters into its highly specialised descendant, Peronospora, an evolutionary absurdity. Runge et al. (2011) suggested that their second alternative, splitting Phytophthora into around six new genera, would be most appropriate, but only on the highly questionable grounds that it would require fewer name changes. In terms of evolutionary process, their third option, reclassifying all DMs under the parental group Phytophthora would probably be the most logical. However, this would be in conflict with the International Code of Nomenclature for algae, fungi and plants (ICNafp) (Turland et al. 2018), which gives the first described genus Peronospora nomenclatural priority (though this could be overcome by conservation of Phytophthora over Peronospora); and, most importantly, it would ignore the biological realities. Voglmayr (2008) considered that none of the above alternatives would receive broad acceptance, "representing a dilemma for classification". Crous et al. (2021a) have also indicated that "it can be expected that Phytophthora will resolve into several genera in future studies". Whether or not the paraphyly of Phytophthora is considered a genuine problem, that it was necessary for Runge et al. (2011) to propose two different 'solutions' is of concern. In our view this highlights the artificiality and subjectivity of the taxonomic process: such an approach takes little account of the often considerable biological and phylogenetic distances between Phytophthora and the DMs. This raises the question whether paraphyly, the emergence of one distinct life form from another without the progenitor becoming extinct, needs to be resolved by a different taxonomy at all, but should simply be accepted as a common feature of evolution in many ancient and successful genera. Around 20% of animal and 20-50% of plant species are paraphyletic in these terms (Crisp and Chandler 1996;Ross 2014). This makes it a common trait of evolution to be accepted at all taxonomic levels. Indeed, the somewhat negative use of the term 'paraphyly' in cladistics has been characterised as "Disparaging phylogenetic jargon for a cladogram's representation of a progenitor in a macroevolutionary series" (Zander 2013).
Further, in terms of the definitions of Ashlock (1971) and Aubert (2015), based on the original definition of a phylon as the totality of organisms 'related by blood and descended from a common typical ancestor' (Haeckel 1877), Phytophthora is clearly monophyletic because all known Phytophthora species share the same common ancestor; yet Phytophthora is also paraphyletic because it does not contain all descendants of the common ancestor, i.e. it does not include the DMs. Collectively, however, Phytophthora and the DMs are holophyletic, since they contain all the descendants of their shared common ancestor. In contrast to this essentially Darwinian definition of monophyly, cladism does not discriminate between monophyly and holophyly, but focusses the definition of monophyly on the descendants, not on the ancestor as in the original Haeckelian sense (Hennig 1966;Ashlock 1971;Hörandl 2006Hörandl , 2007Aubert 2015). As a consequence, in cladism the terms monophyly and Page 18 of 25 Brasier et al. IMA Fungus (2022) 13:12 paraphyly are sometimes applied to phylogenetic trees as if they describe fixed or immutable entities. In reality they are useful generalisations that attempt to define a complex or continuum but are often unreliable due to past reticulations, significant gaps due to extinctions and, in the case of Phytophthora, the numerous undiscovered taxa (Brasier 2009). This renders the question of applying taxonomic weight, or names, to phylogenetic dichotomies contentious. We consider that the key question for determining an appropriate taxonomy is not the existence of a node, but the evolutionary processes that gave rise to the divergence of the lineages and the extent of the biological changes involved (cf Brasier 2009). This approach takes into account the main geographic, genetic or biological drivers of the dichotomy. Often these can only be retrospectively inferred, rather than critically established. In terms of many analysts (e.g. Ashlock 1971;Crisp and Chandler 1996;Brummit 1998;Mayr and Bock 2002;Brummit and Sosef 2003;Hörandl 2006Hörandl , 2007Zander 2013;Aubert 2015), this is an evolutionary as opposed to a purely cladistic approach to establishing a meaningful and practical, if still approximate, taxonomy; and one in which classification is not allowed to trump evolution. Zander (2013) has pithily summarised this viewpoint as follows: Phylogenetics imposes a classification on the results of cladistic analysis without a process-based explanation of those results. The sister-group structure is taken to be a classification itself. Evolution is not clustering, classification is. Evolution is not nesting, classification is. Phylogenetics leaps from the clustering and nesting of cladistic analysis straight to classification without explanation of the analysis in terms of serial transformations of one taxon into another, which is the nut of (Darwinian) macroevolutionary theory.
On the above basis and taking into account our suggestions regarding the post-Gondwanan expansion of the Phytophthora clades, we consider Phytophthora to be a fundamentally monophyletic cluster that has at least twice given rise to the evolution of descendants with a distinct set of biological traits linked to obligate biotrophy, the DMs, via paraphyletic 'jumps' . Since such jumps are common in nature, we see no current biological justification or systematic need for subjecting Phytophthora, a successful, ancient and biologically coherent mother genus, to segregation into separate genera. Further, proposals to do so appear mainly to be a device to address the convergent evolution of the DMs rather than a problem related to the structure of Phytophthora per se. This, despite the fact that it has also been acknowledged by Crous et al. (2021b) that, as a unit, a 'genus' should be defined not only by phylogeny but also by common morphological, ecological and chemical properties (= synapomorphies).
Further, because of their substantial differences in lifestyle, we consider it appropriate to accept a much broader generic concept for Phytophthora than for the DMs. In the more morphologically limited and behaviourally specialized DMs, genera have tended to be discriminated by conidiosporangial pigmentation and conidiophore and haustorial morphology, host specificity and, more recently, phylogenetic separation (e.g. Göker et al. 2003Göker et al. , 2007Voglmayer 2008;Thines et al. 2015). For example, the BDM genus Hyaloperonospora is distinguished from the DMCC genus Peronospora largely by globose haustoria, non-pigmentation of the conidial walls and brassicaceous versus broad host specialisation. The other BDM genus, Perofacia, is distinguished from Hyaloperonospora largely by uniformly ellipsoidal conidia and the pseudodichotomous and appressed conidiophores (Constantinescu and Fatehi 2002). These generic differences are even more limited than the differences between some phylogenetically very closely related Phytophthora species. Thus P. ramorum and P. hibernalis in Phytophthora Clade 8c differ in sporangial pedicel morphology, the presence of chlamydospores, breeding system, antheridial type, oospore size, optimum temperature for growth and their main host families.
Overall, we consider that the biological and evolutionary case for retaining Phytophthora as a single genus is overwhelming. We have already shown that the 11 major Phytophthora clades share a characteristic diversity and plasticity across an extensive suite of morphological features, breeding systems and lifestyles. While there are trends, none of the clades are distinguished by a unique special character (synapomorphy) or combination of characters (cf. Bennett et al. 2017). In addition to monophyly, we consider the latter should be an indispensable requirement for recognition of a separate genus. Consequently, we propose for Phytophthora, rather than a monophyly-centred cladistic concept, a more 'Darwinian ' generic concept based on similarity (synapomorphies) and common descent (monophyly in the original Haeckelian sense; Mayr and Bock 2002;Hörandl 2006). This allows similarities within the older parental group (Phytophthora) which exists in parallel to the descendent group (DMs) while excluding similarities resulting solely from convergent evolution.

Scientific communication and biosecurity importance of Phytophthora as a cohesive genus
Through being both well biologically defined and widely accepted the generic name Phytophthora is currently an engine of understanding and communication for a large body of scientists operating across disciplines ranging Page 19 of 25 Brasier et al. IMA Fungus (2022) 13:12 from mycology and plant pathology to biosecurity and social history. This wider 'Phytophthora community' has, over time, not only generated dedicated books (e.g. Erwin et al. 1983;Lucas et al. 1991;Erwin and Ribeiro 1996;Lamour 2013) but an enormous scientific literature base. Currently there are ca 14,000 articles in Scopus (compared with ca 4000 for all 20 DM genera combined), and that literature continues to grow rapidly. This unifying scientific communication value would be seriously damaged by an inappropriate and unnecessary attempt to break up the genus. The impact on biosecurity needs to be seen in the context of the extensive damage caused by Phytophthoras to cash crops and forests (Tables 2, 3, Additional files 1, 2: Tables S1, S2); the new epidemics and pandemics resulting from introductions of exotic Phytophthoras via international trade in plants and international travel (Fig. 2); and the many new Phytophthora species being discovered in underexplored ecosystems with the potential to cause further pandemics, especially in host plants they have not previously encountered. Because of these threats, coherent unambiguous communication about the genus is extremely important for developing sound, evidence-based biosecurity and plant health protocols at both the international and local scale. The current understanding among regulators and scientists about what is meant by Phytophthora when developing plant health regulation is a valuable asset in crop and habitat protection. An unnecessarily designation of multiple new genera could seriously damage this understanding, resulting in confusion and, at worse, weakened biosecurity, adding another threat to an already fragile global environment. These problems would probably be further exacerbated by the often long time lags between taxonomic changes and names being incorporated into plant health legislation or into extension programmes.
Regarding the scope for engendering confusion, many natural and managed ecosystems are inhabited by multiple Phytophthora species. For example, 27 and 39 Phytophthora species respectively, from seven clades in each case, have recently been found in the forests and natural ecosystems of Taiwan and Vietnam (Brasier et al. 2010;Jung et al. 2017bJung et al. , d, 2020; while horticultural nurseries across Europe are infested by at least 65 Phytophthora taxa from nine clades (Table 3, Additional file 2: Table S2; Moralejo et al. 2009;Jung et al. 2016). Moreover, the same disease syndromes are often caused by multiple Phytophthoras. At least 26 Phytophthora species from nine clades are associated with the current pan-European declines of oak forests (Table 3, Additional file 2: Table S2); and at least 51 species and hybrids are associated with damage to native plant communities around San Francisco (Table 3, Additional file 2: Table S2). So common are Phytophthoras on trees that commercial lateral flow devices are available to diagnose the genus (e.g. Tomlinson et al. 2010). Any designation of new genera that unnecessarily dissected the common biological properties of Phytophthoras would negatively impact communication and management in these and many similar situations and cause confusion among practitioners such as farmers, horticulturalists, forest managers and nursery owners reliant on scientific extension programmes for guidance.
The potential impact on verbal discourse deserves its own consideration. At a recent meeting of pathologists, forest health surveyors and plant health regulators in Britain addressing a previously unrecorded Phytophthora attacking Western Hemlock (Tsuga heterophylla) (Pérez-Sierra et al. 2022), discussion ranged across ten forest Phytophthora species from six different clades. To have referred to these by multiple generic names would have rendered the discussion unnecessarily complex and confusing to taxonomists and non-taxonomists alike. Similarly, upwards of 70 Phytophthora species across all 11 major clades are routinely discussed at the biennial International Forest Phytophthora Symposia. These meetings are an important channel of communication at a time of major Phytophthora threats to forests and natural ecosystems. Any unnecessary break-up of the genus would seriously undermine the value and purpose of this research community.
Numerous Government and NGO websites worldwide are dedicated to Phytophthora threats (e.g. Anonymous 1-4). Furthermore, terms such as 'Phytophthora dieback' , 'Phytophthora decline' 'Phytophthora root rot' , 'Phytophthora collar rot' , 'Phytophthora leaf blight' and 'Phytophthora bleeding canker' are used widely in books, scientific papers and at meetings to discriminate the main disease syndromes common across the Phytophthora clades. The differences of meaning between the terms are well understood by academic plant pathologists, field surveyors and plant health regulators alike. In Britain and Australia terms such as 'Phytophthora root rot' and 'Phytophthora dieback' are even in common usage in horticultural magazines and the popular media. Broadly, these terms are an important component of the language centred around Phytophthora behaviour, disease management and biosecurity.
The risks to effective scientific communication inherent in over-zealous application of formal taxonomic practices in the context of molecular phylogenetics can be seen in the recent debate around Fusarium, another historic pathogen genus of high biosecurity importance. Regrettably, there now appears to be a damaging split in the international Fusarium community over what does, and does not, constitute the genus (Crous et al. 2021b;Page 20 of 25 Brasier et al. IMA Fungus (2022) 13:12 Geiser et al. 2021). A similar damaging controversy centred recently on the issue of whether to split the genus Aspergillus into multiple genera (Pitt and Taylor 2016) or retain it as a single genus (Samson et al. 2017).

CONCLUSIONS AND RECOMMENDATIONS
Arguably Phytophthora remains one of, if not the bestknown and most important genus of plant pathogens. Despite the rapid increase in the number of described Phytophthora species and improvements in molecular phylogeny the genus has remained structurally coherent and biologically well understood. In our view, no one Phytophthora major clade or combination of clades exhibits a sufficiently distinct set of biological characteristics to warrant a unique generic status. Paraphyletic jumps, such as the emergence of the DMs from Phytophthora ancestors, should be considered a normal feature of evolution in ancient and successful genera such as this. Enthusiasm to 'dice and slice' along the lines of cladistic nuances should not trump evolutionary or biological coherence or overlook the fact that the primary purpose of names is to facilitate communication.
We are aware that under the orthodoxies, idiosyncrasies and sometimes vague constructs of the ICNafp (cf. Hawksworth 2020) a taxonomic restructuring of Phytophthora could be published relatively unchallenged by any author or group regardless of their familiarity with the genus as long as they follow certain somewhat subjective rules. 'Phytophthora' is surely now bigger than all of us. In which case its status needs to be policed by a wide consensus of the scientific community, perhaps through a recommendation of a working group of the International Commission on the Taxonomy of Fungi (ICFT). We contend therefore that any proposal for a major restructuring of the circumscription of the genus should be presented to and considered by an international working group of Phytophthora researchers, perhaps under ICTF auspices. There are already strong precedents for the international community coming together on aspects of Phytophthora research. For example, an international meeting debated the case 'for or against diploidy in Phytophthora' at the University of Bari, Italy in May 1972 (Brasier 2008); and there have been large International Symposia on Phytophthora at the University of California, Riverside in 1982 (Erwin et al. 1983) and at Trinity College, Dublin in 1989 (Lucas et al. 1991). The issue might also be usefully addressed by a special session during the next International Mycological Congress in Maastricht in 2024.
While a case might be made for assigning sub-generic or section names to the various Phytophthora clades, as is the practice in some other large genera such as Agaricus, Aspergillus, Cladonia, Hebeloma and Penicillium, we doubt this would add much to our communication or understanding, and could be even more confusing to end users.
Considering all the above issues, and especially the lack of unequivocal evidence that defining Phytophthora clades as discrete genera would result in more biologically meaningful entities, we recommend that the current broad generic concept be retained. This would preserve the cultural history of the genus. It would also maintain the currently enormously effective value of the name Phytophthora in scientific communication, including for the many applied biologists and regulators dealing with Phytophthoras on a daily basis.